Cited by 351Origins and Evolution of LifeGenomics and Phylogenetic StudiesBacterial Genetics and Biotechnology

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Did DNA replication evolve twice independently?

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Leipe, D. D., Aravind, L., Koonin, E. V.·1999·Nucleic Acids Research

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Abstract

DNA replication is central to all extant cellular organisms. There are substantial functional similarities between the bacterial and the archaeal/eukaryotic replication machineries, including but not limited to defined origins, replication bidirectionality, RNA primers and leading and lagging strand synthesis. However, several core components of the bacterial replication machinery are unrelated or only distantly related to the functionally equivalent components of the archaeal/eukaryotic replication apparatus. This is in sharp contrast to the principal proteins involved in transcription and translation, which are highly conserved in all divisions of life. We performed detailed sequence comparisons of the proteins that fulfill indispensable functions in DNA replication and classified them into four main categories with respect to the conservation in bacteria and archaea/eukaryotes: (i) non-homologous, such as replicative polymerases and primases; (ii) containing homologous domains but apparently non-orthologous and conceivably independently recruited to function in replication, such as the principal replicative helicases or proofreading exonucleases; (iii) apparently orthologous but poorly conserved, such as the sliding clamp proteins or DNA ligases; (iv) orthologous and highly conserved, such as clamp-loader ATPases or 5'-->3' exonucleases (FLAP nucleases). The universal conservation of some components of the DNA replication machinery and enzymes for DNA precursor biosynthesis but not the principal DNA polymerases suggests that the last common ancestor (LCA) of all modern cellular life forms possessed DNA but did not replicate it the way extant cells do. We propose that the LCA had a genetic system that contained both RNA and DNA, with the latter being produced by reverse transcription. Consequently, the modern-type system for double-stranded DNA replication likely evolved independently in the bacterial and archaeal/eukaryotic lineages.

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Whitfield, J. (2006) · Nature · doi:10.1038/439130a · Cited by 5
‘Parabiotic Evolution’: From Stochasticity in Geochemical and Subsequent Processes to Genes, Genomes and Modular CellsPreprint
Egel, R. (2017) · Preprints.org · doi:10.20944/preprints201710.0153.v1 · Cited by 5
Universal paralogs provide a window into evolution before the last universal common ancestor
Goldman, A. D., Fournier, G. P., & Kaçar, B. (2026) · Cell Genomics · doi:10.1016/j.xgen.2026.101140 · Cited by 5
“20 The LUCA also appears to have encoded a nearly complete translation system similar to those seen across the biosphere today, including a complete ribosome, 21,22 the canonical genetic code, 23–25 and core translation-related proteins.”
The time of appearance of the genetic code
Giulio, M. D. (2024) · Biosystems · doi:10.1016/j.biosystems.2024.105159 · Cited by 4
Domain Structures and Inter-Domain Interactions Defining the Holoenzyme Architecture of Archaeal D-Family DNA Polymerase
Matsui, I., Matsui, E., Yamasaki, K., & Yokoyama, H. (2013) · Life · doi:10.3390/life3030375 · Cited by 4
“Replicative DNA polymerases (DNA Pols) are divided into archaeal-eukaryotic and bacterial types that appear not to be homologous to each other [1,2].”
Evolutionary origin of B family DNA-dependent DNA polymerases from retrotranscriptases
de Farías, S. T., Furtado, A. N. M., dos Santos, A. P., & José, M. V. (2023) · Biosystems · doi:10.1016/j.biosystems.2023.104963 · Cited by 4
Modelling evolution on design-by-contract predicts an origin of Life through an abiotic double-stranded RNA world
Roos, A. D. G. D. (2007) · Biology Direct · doi:10.1186/1745-6150-2-12 · Cited by 4
“an RNA template to dsDNA, possibly by a dsRNA intermediate [9,10].”
Background
Disordered interdomain region of Gins is important for functional tetramer formation to stimulate MCM helicase in Thermoplasma acidophilum
Ogino, H., Ishino, S., Oyama, T., et al. (2014) · Bioscience Biotechnology and Biochemistry · doi:10.1080/09168451.2014.982503 · Cited by 4
The Last Common Ancestor of Modern Cells
Moreira, D., & López‐García, P. (2007) · Springer eBooks · doi:10.1007/978-3-540-33693-8_11 · Cited by 4
“According to this model, the cenancestor would have had an RNA genome, and DNA replication would have evolved twice independently, once in the bacterial line of descent and other in the lineage leading to archaea and eukaryotes (Forterre 2002; Leipe et al. 1999 ).”
Method
Looking for the Most ‘Primitive’ Life Forms: Pitfalls and Progresses
Gribaldo, S., & Forterre, P. (2005) · Advances in astrobiology and biogeophysics · doi:10.1007/10913406_18 · Cited by 4
Dielectricity of a molecularly crowded solution accelerates NTP misincorporation during RNA-dependent RNA polymerization by T7 RNA polymerase
Takahashi, S., Matsumoto, S., Chilka, P., Ghosh, S., Okura, H., & Sugimoto, N. (2022) · Scientific Reports · doi:10.1038/s41598-022-05136-8 · Cited by 4
An Overview on Natively Unfolded Proteins
Nishikawa, K. (2009) · Seibutsu Butsuri · doi:10.2142/biophys.49.004 · Cited by 3
Two RNA Worlds: Toward the Origin of Replication, Genes, Recombination, and Repair
Lankenau, D. (2011) · Springer eBooks · doi:10.1007/978-3-642-21625-1_11 · Cited by 3
Cryo‐EM of dynamic protein complexes in eukaryotic DNA replication
Sun, J., Yuan, Z., Bai, L., & Li, H. (2016) · Protein Science · doi:10.1002/pro.3033 · Cited by 3
“Thanks to the recent advance in direct electron detection technology and image processing methods, cryo-EM is now a high resolution structural tool that is complementary to X-ray crystallography and NMR.1–3 In the cases of membrane proteins and large protein complexes, cryo-EM is particularly advantageous over other m…”
Background
A Model for the Evolution of Nucleotide Polymerase Directionality
Ballanco, J., & Mansfield, M. L. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018881 · Cited by 4
“While this is the most we can conclude from the evidence presented here, combined with other evidence that the machinery involved in DNA polymerization evolved at least twice independently [9], the weight of evidence favors the explanation that evolutionary competition was the driving factor in determining the modern…”
Background
Mutual interaction enables the mycobacterial plasmid pAL5000 origin binding protein RepB to recruit RepA, the plasmid replicase, to the origin
Chatterjee, S., Patra, M. M., Samaddar, S., et al. (2017) · Microbiology · doi:10.1099/mic.0.000447 · Cited by 3
“Despite the similarity, the proteins involved in executing the processes do not appear to be evolutionarily related [2].”
Background
Did an Early Version of the Eukaryal Replisome Enable the Emergence of Chromatin?
Kaufmann, G., & Nethanel, T. (2004) · Progress in nucleic acid research and molecular biology · doi:10.1016/s0079-6603(04)77005-1 · Cited by 3
DNA translocation by the CMG helicase: the helical inchworm model
Batra, S., Allwein, B., Wang, Y. L., Hite, R. K., & Remus, D. (2026) · Biochemical Society Transactions · doi:10.1042/bst20250145 · Cited by 2
“CMG’s distinct translocation mechanism likely stems from the deep evolutionary divergence of hexameric helicases, which gave rise to structural variations that may underpin mechanistic differences [1,61].”
The Possible Crystallization Process in the Origin of Bacteria, Archaea, Viruses, and Mobile Elements
Yoshimura, A., & Seki, M. (2024) · Biology · doi:10.3390/biology14010003 · Cited by 1
“Thus, the equivalent replication components of the σ genome and TBP genome were no longer exchangeable, leading to a complete DNA replication divide between Bacteria and Archaea (Figure 5D(c)) [60].”
DNA Replication in Time and Space: The Archaeal Dimension
Serdyuk, A., & Allers, T. (2025) · DNA · doi:10.3390/dna5020024 · Cited by 2
“Anand [160] emphasizes the lack of progress in understanding the conversion of D-loop structures into replisomes in BIR of [148], where the 3 ′ end of the DNA strand from the previous replication cycle is used to prime and initiate the next round of replication, thus the mechanism is described as…”
DNA Replication in Archaea, the Third Domain of Life
Ishino, Y., & Ishino, S. (2013) · InTech eBooks · doi:10.5772/53986 · Cited by 2
“[155] Wilkinson A, Day J, Bowater R. Bacterial DNA ligases.”
BackgroundInfluential
Biochemical Characterization of a Mycobacteriophage Derived DnaB Ortholog Reveals New Insight into the Evolutionary Origin of DnaB Helicases
Bhowmik, P., & GUPTA, S. K. (2015) · PLoS ONE · doi:10.1371/journal.pone.0134762 · Cited by 2
“Replicative helicases of organisms belonging to the two other domains of life–Archaea and Eukarya are evolutionarily unrelated to DnaB (non-orthologous) and do not belong to the RecA superfamily [14, 28].”
Background
Consequences of EPR–Proton Qubits Populating DNA
Cooper, W. G. (2018) · Advances in quantum chemistry · doi:10.1016/bs.aiq.2017.12.001 · Cited by 2
Reconstructing the Last Universal Common Ancestor
Poole, A. M. (2021) · Advances in astrobiology and biogeophysics · doi:10.1007/978-3-030-81039-9_9 · Cited by 4
Telomeres in Evolution and Development from Biosemiotic PerspectivePreprint
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Authors: Leipe, D. D., Aravind, L., & Koonin, E. V.
Affiliations: National Institutes of Health (US)
Texas A&M University (US)
Corresponding author: Koonin, E. V.
ORCID: Aravind, L.
Koonin, E. V.
Venue: Nucleic Acids Research
Publisher: Oxford University Press (OUP)
Published: 1999-09-01
Volume: 27
Issue: 17
Pages: 3389-3401
ISSN: 0305-1048 (ISSN-L)
1362-4962
DOI: 10.1093/nar/27.17.3389
PMC: PMC148579
OpenAlex: W2018024025
Semantic Scholar: 9f9be31d2a06621cfbcaa7642db469b8cea929dc
Cited by: 351
References: 66
Citations by year: 2026: 6 · 2025: 5 · 2024: 16 · 2023: 5 · 2022: 5 · 2021: 11 · 2020: 10 · 2019: 6 · 2018: 12 · 2017: 13 · 2016: 15 · 2015: 13 · 2014: 18 · 2013: 12 · 2012: 5
FWCI: 13.34
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Nucleic Acids Research (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords: DNA replication, origin of replication, convergent evolution, last common ancestor, primase, replicative helicase, proofreading exonuclease, DNA ligase, RNA-DNA hybrids, reverse transcription, sequence conservation
MeSH terms: Animals, Bacterial Proteins, Cytoplasm, DNA Replication, Drosophila, Fungal Proteins, Models, Genetic, Sequence Homology, Nucleic Acid, Databases, Factual, Sequence Analysis, DNA, Evolution, Molecular, Archaeal Proteins

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Did DNA replication evolve twice independently?

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